The composition of cuticular compounds indicates body parts, sex and age in the model butterfly Bicyclus anynana (Lepidoptera)

Abstract

Chemical communication in insects' sexual interactions is well-known to involve olfaction of volatile compounds called sex pheromones. In theory, sexual chemical communication may also involve chemicals with low or no volatility exchanged during precopulatory gustatory contacts. Yet, knowledge on this latter type of chemicals is so far mostly restricted to the Drosophila fly model. Here we provide the most comprehensive characterization to date of the cuticular chemical profile, including both volatile and non-volatile compounds, of a model butterfly, Bicyclus anynana. First, we characterized the body distribution of 103 cuticular lipids, mostly alkanes and methyl-branched alkanes, by gas chromatography coupled to mass spectrometry (GC-MS). Second, we developed a multivariate statistical approach to cope with such complex chemical profiles and showed that variation in the presence or abundance of a subset of the cuticular lipids indicated body parts, and traits involved in B. anynana mate choice, namely sex and age. Third, we identified the chemical structure of the 20 most indicative compounds, which were on average more abundant (1346.4 ± 1994.6 ng; mean ± SD) than other, likely less indicative, compounds (225.9 ± 507.2 ng; mean ± SD). Fourth, we showed that wings and legs displayed most of the chemical information found on the entire body of the butterflies. Fifth, we showed that non-random gustatory contacts occurred between specific male and female body parts during courtship. The body parts mostly touched by the conspecific displayed the largest between-sex differentiation in cuticular composition. Altogether, the large diversity of cuticular lipids in B. anynana, which exceeds the one of Drosophila flies, and its non-random distribution and evaluation across individuals, together suggest that gustatory information is likely exchanged during sexual interactions in Lepidoptera.

Beyond magic traits: Multimodal mating cues inHeliconiusbutterflies

“…Together with the recent results on cuticular compounds in B. anynana (Heuskin et al. ), as well as former studies on Argynnis , and longstanding observations of mating behavior at short range, our study calls for assessing the relevance of female chemical cues for intraspecific and interspecific sexual interactions not only in moths but also in butterflies.…”

“…In another butterfly species, Bicyclus anynana , the composition of cuticular compounds in females differs between body parts and covaries with age (Heuskin et al. ). Our experiments with hybrid females show that the intensity of H. timareta male courtship is correlated with chemical composition of the presented female, supporting that male courtship decision relies on particular and species‐divergent female chemical cues.…”

“…Following Heuskin et al. () and Lecocq et al. (), we used the indval index, usually used for ecological data as an estimator of the association between species abundance and an ecological factor.…”

Dense, small and male-biased cages exacerbate male–male competition and reduce female choosiness in Bicyclus anynana

“…1). We used 8e10-day-old virgin males as all three components of the male sex pheromone, which is a major secondary sexual trait under sexual selection, are present at significant levels in the male blend at this age (Heuskin et al, 2014;Nieberding et al, 2008Nieberding et al, , 2012. We used 3e5-day-old virgin females as they readily mate in the laboratory (Brakefield et al, 2009;Nieberding et al, 2008Nieberding et al, , 2012.…”

The Long and the Short of Mate Attraction in a Psylloid: do Semiochemicals Mediate Mating in Aacanthocnema dobsoni Froggatt?

“…Despite growing evidence that these compounds provide essential protection against desiccation and are used for communication in taxa such as Hymenoptera, Coleoptera, and Lepidoptera (Guerrieri et al 2009; Heuskin et al 2014; Zhang et al 2014, little is known about the nature and biological function of CHCs in Psylloidea. We have shown that the CHC profile of A. dobsoni is dominated by n alkanes, monomethyl , and dimethyl alkanes.…”